Plectin sidearms mediate interaction of intermediate filaments with microtubules and other components of the cytoskeleton

doi:10.1083/jcb.135.4.991

Quantitative Colocalization Analysis Software

This Article

	Full Text (PDF, 12645K)
	Alert me when this article is cited
	Citation Map

Services

	Email this article
	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new content in the JCB
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Svitkina, T. M.
	Articles by Borisy, G. G.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Svitkina, T. M.
	Articles by Borisy, G. G.


Social Bookmarking

	What's this?

ARTICLES

Plectin sidearms mediate interaction of intermediate filaments with microtubules and other components of the cytoskeleton

TM Svitkina, AB Verkhovsky and GG Borisy
Laboratory of Molecular Biology, University of Wisconsin, Madison 53706, USA. tsvitkin@facstaff.wisc.edu

By immunogold labeling, we demonstrate that "millipede-like" structures seen previously in mammalian cell cytoskeletons after removal of actin by treatment with gelsolin are composed of the cores of vimentin IFs with sidearms containing plectin. These plectin sidearms connect IFs to microtubules, the actin-based cytoskeleton and possibly membrane components. Plectin binding to microtubules was significantly increased in cells from transgenic mice lacking IFs and was reversed by microinjection of exogenous vimentin. These results suggest the existence of a pool of plectin which preferentially associates with IFs but may also be competed for by microtubules. The association of IFs with microtubules did not show a preference for Glu-tubulin. Nor did it depend upon the presence of MAP4 since plectin links were retained after specific immunodepletion of MAP4. The association of IFs with stress fibers survived actin depletion by gelsolin suggesting that myosin II minifilaments or components closely associated with them may play a role as plectin targets. Our results provide direct structural evidence for the hypothesis that plectin cross-links elements of the cytoskeleton thus leading to integration of the cytoplasm.
Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Facebook Add to Reddit Reddit Add to Technorati Technorati Twitter What's this?

This article has been cited by other articles:

Yuan, A., Sasaki, T., Rao, M. V., Kumar, A., Kanumuri, V., Dunlop, D. S., Liem, R. K., Nixon, R. A. (2009). Neurofilaments Form a Highly Stable Stationary Cytoskeleton after Reaching a Critical Level in Axons. J. Neurosci. 29: 11316-11329 [Abstract] [Full Text]
Na, S., Chowdhury, F., Tay, B., Ouyang, M., Gregor, M., Wang, Y., Wiche, G., Wang, N. (2009). Plectin contributes to mechanical properties of living cells. Am. J. Physiol. Cell Physiol. 296: C868-C877 [Abstract] [Full Text]
Yoon, K.-h., FitzGerald, P. G. (2009). Periplakin Interactions with Lens Intermediate and Beaded Filaments. IOVS 50: 1283-1289 [Abstract] [Full Text]
Garcia, M. L., Rao, M. V., Fujimoto, J., Garcia, V. B., Shah, S. B., Crum, J., Gotow, T., Uchiyama, Y., Ellisman, M., Calcutt, N. A., Cleveland, D. W. (2009). Phosphorylation of Highly Conserved Neurofilament Medium KSP Repeats Is Not Required for Myelin-Dependent Radial Axonal Growth. J. Neurosci. 29: 1277-1284 [Abstract] [Full Text]
Mruk, D. D., Silvestrini, B., Cheng, C. Y. (2008). Anchoring Junctions As Drug Targets: Role in Contraceptive Development. Pharmacol. Rev. 60: 146-180 [Abstract] [Full Text]
Ketema, M., Wilhelmsen, K., Kuikman, I., Janssen, H., Hodzic, D., Sonnenberg, A. (2007). Requirements for the localization of nesprin-3 at the nuclear envelope and its interaction with plectin. J. Cell Sci. 120: 3384-3394 [Abstract] [Full Text]
Kim, S., Coulombe, P. A. (2007). Intermediate filament scaffolds fulfill mechanical, organizational, and signaling functions in the cytoplasm. Genes Dev. 21: 1581-1597 [Abstract] [Full Text]
Long, H. A., Boczonadi, V., McInroy, L., Goldberg, M., Maatta, A. (2006). Periplakin-dependent re-organisation of keratin cytoskeleton and loss of collective migration in keratin-8-downregulated epithelial sheets. J. Cell Sci. 119: 5147-5159 [Abstract] [Full Text]
Esue, O., Carson, A. A., Tseng, Y., Wirtz, D. (2006). A Direct Interaction between Actin and Vimentin Filaments Mediated by the Tail Domain of Vimentin. J. Biol. Chem. 281: 30393-30399 [Abstract] [Full Text]
Osmanagic-Myers, S., Gregor, M., Walko, G., Burgstaller, G., Reipert, S., Wiche, G. (2006). Plectin-controlled keratin cytoarchitecture affects MAP kinases involved in cellular stress response and migration. JCB 174: 557-568 [Abstract] [Full Text]
Powell, K. (2005). What the cytoskeleton really looks like. JCB 170: 1019-1019 [Full Text]
Kalinin, A. E., Idler, W. W., Marekov, L. N., McPhie, P., Bowers, B., Steinert, P. M., Steven, A. C. (2004). Co-assembly of Envoplakin and Periplakin into Oligomers and Ca2+-dependent Vesicle Binding: IMPLICATIONS FOR CORNIFIED CELL ENVELOPE FORMATION IN STRATIFIED SQUAMOUS EPITHELIA. J. Biol. Chem. 279: 22773-22780 [Abstract] [Full Text]
Lee, N. P. Y., Mruk, D. D., Conway, A. M., Cheng, C. Y. (2004). Zyxin, Axin, and Wiskott-Aldrich Syndrome Protein Are Adaptors That Link the Cadherin/Catenin Protein Complex to the Cytoskeleton at Adherens Junctions in the Seminiferous Epithelium of the Rat Testis. J Androl 25: 200-215 [Abstract] [Full Text]
Helfand, B. T., Chang, L., Goldman, R. D. (2004). Intermediate filaments are dynamic and motile elements of cellular architecture. J. Cell Sci. 117: 133-141 [Abstract] [Full Text]
Garcia, M. L., Lobsiger, C. S., Shah, S. B., Deerinck, T. J., Crum, J., Young, D., Ward, C. M., Crawford, T. O., Gotow, T., Uchiyama, Y., Ellisman, M. H., Calcutt, N. A., Cleveland, D. W. (2003). NF-M is an essential target for the myelin-directed "outside-in" signaling cascade that mediates radial axonal growth. JCB 163: 1011-1020 [Abstract] [Full Text]
Rao, M. V., Campbell, J., Yuan, A., Kumar, A., Gotow, T., Uchiyama, Y., Nixon, R. A. (2003). The neurofilament middle molecular mass subunit carboxyl-terminal tail domains is essential for the radial growth and cytoskeletal architecture of axons but not for regulating neurofilament transport rate. JCB 163: 1021-1031 [Abstract] [Full Text]
Gilles, C., Polette, M., Mestdagt, M., Nawrocki-Raby, B., Ruggeri, P., Birembaut, P., Foidart, J.-M. (2003). Transactivation of Vimentin by {beta}-Catenin in Human Breast Cancer Cells. Cancer Res. 63: 2658-2664 [Abstract] [Full Text]
Liovic, M., Mogensen, M. M., Prescott, A. R., Lane, E. B. (2003). Observation of keratin particles showing fast bidirectional movement colocalized with microtubules. J. Cell Sci. 116: 1417-1427 [Abstract] [Full Text]
Goriounov, D., Leung, C. L., Liem, R. K. H. (2003). Protein products of human Gas2-related genes on chromosomes 17 and 22 (hGAR17 and hGAR22) associate with both microfilaments and microtubules. J. Cell Sci. 116: 1045-1058 [Abstract] [Full Text]
Karashima, T., Watt, F. M. (2003). Interaction of periplakin and envoplakin with intermediate filaments. J. Cell Sci. 115: 5027-5037 [Abstract] [Full Text]
Davies, P. F., Zilberberg, J., Helmke, B. P. (2003). Spatial Microstimuli in Endothelial Mechanosignaling. Circ. Res. 92: 359-370 [Abstract] [Full Text]
Rao, M. V., Engle, L. J., Mohan, P. S., Yuan, A., Qiu, D., Cataldo, A., Hassinger, L., Jacobsen, S., Lee, V. M-Y., Andreadis, A., Julien, J.-P., Bridgman, P. C., Nixon, R. A. (2002). Myosin Va binding to neurofilaments is essential for correct myosin Va distribution and transport and neurofilament density. JCB 159: 279-290 [Abstract] [Full Text]
Larsen, A.-K. R., Moller, M. T. N., Blankson, H., Samari, H. R., Holden, L., Seglen, P. O. (2002). Naringin-sensitive Phosphorylation of Plectin, a Cytoskeletal Cross-linking Protein, in Isolated Rat Hepatocytes. J. Biol. Chem. 277: 34826-34835 [Abstract] [Full Text]
Rao, M. V., Garcia, M. L., Miyazaki, Y., Gotow, T., Yuan, A., Mattina, S., Ward, C. M., Calcutt, N. A., Uchiyama, Y., Nixon, R. A., Cleveland, D. W. (2002). Gene replacement in mice reveals that the heavily phosphorylated tail of neurofilament heavy subunit does not affect axonal caliber or the transit of cargoes in slow axonal transport. JCB 158: 681-693 [Abstract] [Full Text]
Beil, M., Leser, J., Lutz, M. P., Gukovskaya, A., Seufferlein, T., Lynch, G., Pandol, S. J., Adler, G. (2002). Caspase 8-mediated cleavage of plectin precedes F-actin breakdown in acinar cells during pancreatitis. Am. J. Physiol. Gastrointest. Liver Physiol. 282: G450-G460 [Abstract] [Full Text]
Shafrir, Y., Forgacs, G. (2002). Mechanotransduction through the cytoskeleton. Am. J. Physiol. Cell Physiol. 282: C479-C486 [Abstract] [Full Text]
Lee, S., Kolodziej, P. A. (2002). Short Stop provides an essential link between F-actin and microtubules during axon extension. Development 129: 1195-1204 [Abstract] [Full Text]
Brown, M. J., Hallam, J. A., Liu, Y., Yamada, K. M., Shaw, S. (2001). Cutting Edge: Integration of Human T Lymphocyte Cytoskeleton by the Cytolinker Plectin. J. Immunol. 167: 641-645 [Abstract] [Full Text]
Yoon, K. H., Yoon, M., Moir, R. D., Khuon, S., Flitney, F. W., Goldman, R. D. (2001). Insights into the Dynamic Properties of Keratin Intermediate Filaments in Living Epithelial Cells. JCB 153: 503-516 [Abstract] [Full Text]
Gao, Y.-s., Sztul, E. (2001). A Novel Interaction of the Golgi Complex with the Vimentin Intermediate Filament Cytoskeleton. JCB 152: 877-894 [Abstract] [Full Text]
Fontao, L., Geerts, D., Kuikman, I., Koster, J., Kramer, D., Sonnenberg, A. (2001). The interaction of plectin with actin: evidence for cross-linking of actin filaments by dimerization of the actin-binding domain of plectin. J. Cell Sci. 114: 2065-2076 [Abstract] [Full Text]
Fuchs, E., Karakesisoglou, I. (2001). Bridging cytoskeletal intersections. Genes Dev. 15: 1-14 [Full Text]
Sun, D, Leung, C., Liem, R. (2001). Characterization of the microtubule binding domain of microtubule actin crosslinking factor (MACF): identification of a novel group of microtubule associated proteins. J. Cell Sci. 114: 161-172 [Abstract]
Shah, J. V., Flanagan, L. A., Janmey, P. A., Leterrier, J.-F. (2000). Bidirectional Translocation of Neurofilaments along Microtubules Mediated in Part by Dynein/Dynactin. Mol. Biol. Cell 11: 3495-3508 [Abstract] [Full Text]
Waterman-Storer, C., Duey, D. Y., Weber, K. L., Keech, J., Cheney, R. E., Salmon, E.D., Bement, W. M. (2000). Microtubules Remodel Actomyosin Networks in Xenopus Egg Extracts via Two Mechanisms of F-Actin Transport. JCB 150: 361-376 [Abstract] [Full Text]
Wang, N., Stamenovic, D. (2000). Contribution of intermediate filaments to cell stiffness, stiffening, and growth. Am. J. Physiol. Cell Physiol. 279: C188-C194 [Abstract] [Full Text]
Webster, D. R., Patrick, D. L. (2000). Beating rate of isolated neonatal cardiomyocytes is regulated by the stable microtubule subset. Am. J. Physiol. Heart Circ. Physiol. 278: H1653-H1661 [Abstract] [Full Text]
Helmke, B. P., Goldman, R. D., Davies, P. F. (2000). Rapid Displacement of Vimentin Intermediate Filaments in Living Endothelial Cells Exposed to Flow. Circ. Res. 86: 745-752 [Abstract] [Full Text]
Karakesisoglou, I., Yang, Y., Fuchs, E. (2000). An Epidermal Plakin That Integrates Actin and Microtubule Networks at Cellular Junctions. JCB 149: 195-208 [Abstract] [Full Text]
Hein, S., Kostin, S., Heling, A., Maeno, Y., Schaper, J. (2000). The role of the cytoskeleton in heart failure. Cardiovasc Res 45: 273-278 [Abstract] [Full Text]
Shafrir, Y, ben-Avraham, D, Forgacs, G (2000). Trafficking and signaling through the cytoskeleton: a specific mechanism. J. Cell Sci. 113: 2747-2757 [Abstract]
Nievers, M., Kuikman, I, Geerts, D, Leigh, I., Sonnenberg, A (2000). Formation of hemidesmosome-like structures in the absence of ligand binding by the (alpha)6(beta)4 integrin requires binding of HD1/plectin to the cytoplasmic domain of the (beta)4 integrin subunit. J. Cell Sci. 113: 963-973 [Abstract]
Leung, C. L., Sun, D., Zheng, M., Knowles, D. R., Liem, R. K.H. (1999). Microtubule Actin Cross-Linking Factor (Macf): A Hybrid of Dystonin and Dystrophin That Can Interact with the Actin and Microtubule Cytoskeletons. JCB 147: 1275-1286 [Abstract] [Full Text]
Geerts, D., Fontao, L., Nievers, M. G., Schaapveld, R. Q.J., Purkis, P. E., Wheeler, G. N., Lane, E. B., Leigh, I. M., Sonnenberg, A. (1999). Binding of Integrin {alpha}6{beta}4 to Plectin Prevents Plectin Association with F-Actin but Does Not Interfere with Intermediate Filament Binding. JCB 147: 417-434 [Abstract] [Full Text]
Correia, I., Chu, D., Chou, Y.-H., Goldman, R. D., Matsudaira, P. (1999). Integrating the Actin and Vimentin Cytoskeletons: Adhesion-Dependent Formation of Fimbrin-Vimentin Complexes in Macrophages. JCB 146: 831-842 [Abstract] [Full Text]
Svitkina, T. M., Borisy, G. G. (1999). Arp2/3 Complex and Actin Depolymerizing Factor/Cofilin in Dendritic Organization and Treadmilling of Actin Filament Array in Lamellipodia. JCB 145: 1009-1026 [Abstract] [Full Text]
Kreitzer, G., Liao, G., Gundersen, G. G. (1999). Detyrosination of Tubulin Regulates the Interaction of Intermediate Filaments with Microtubules In Vivo via a Kinesin-dependent Mechanism. Mol. Biol. Cell 10: 1105-1118 [Abstract] [Full Text]
Leung, C. L., Sun, D., Liem, R. K.H. (1999). The Intermediate Filament Protein Peripherin Is the Specific Interaction Partner of Mouse BPAG1-n (Dystonin) in Neurons. JCB 144: 435-446 [Abstract] [Full Text]
Gilles, C, Polette, M, Zahm, J., Tournier, J., Volders, L, Foidart, J., Birembaut, P (1999). Vimentin contributes to human mammary epithelial cell migration. J. Cell Sci. 112: 4615-4625 [Abstract]
Yabe, J., Pimenta, A, Shea, T. (1999). Kinesin-mediated transport of neurofilament protein oligomers in growing axons. J. Cell Sci. 112: 3799-3814 [Abstract]
Sider, J., Mandato, C., Weber, K., Zandy, A., Beach, D, Finst, R., Skoble, J, Bement, W. (1999). Direct observation of microtubule-f-actin interaction in cell free lysates. J. Cell Sci. 112: 1947-1956 [Abstract]
Hijikata, T, Murakami, T, Imamura, M, Fujimaki, N, Ishikawa, H (1999). Plectin is a linker of intermediate filaments to Z-discs in skeletal muscle fibers. J. Cell Sci. 112: 867-876 [Abstract]
Gregory, S. L., Brown, N. H. (1998). kakapo, a Gene Required for Adhesion Between and Within Cell Layers in Drosophila, Encodes a Large Cytoskeletal Linker Protein Related to Plectin and Dystrophin. JCB 143: 1271-1282 [Abstract] [Full Text]
Andrä, K., Nikolic, B., Stöcher, M., Drenckhahn, D., Wiche, G. (1998). Not just scaffolding: plectin regulates actin dynamics in cultured cells. Genes Dev. 12: 3442-3451 [Abstract] [Full Text]
Rao, M. V., Houseweart, M. K., Williamson, T. L., Crawford, T. O., Folmer, J., Cleveland, D. W. (1998). Neurofilament-dependent Radial Growth of Motor Axons and Axonal Organization of Neurofilaments Does Not Require the Neurofilament Heavy Subunit (NF-H) or Its Phosphorylation. JCB 143: 171-181 [Abstract] [Full Text]
Yoon, M., Moir, R. D., Prahlad, V., Goldman, R. D. (1998). Motile Properties of Vimentin Intermediate Filament Networks in Living Cells. JCB 143: 147-157 [Abstract] [Full Text]
Prahlad, V., Yoon, M., Moir, R. D., Vale, R. D., Goldman, R. D. (1998). Rapid Movements of Vimentin on Microtubule Tracks: Kinesin-dependent Assembly of Intermediate Filament Networks. JCB 143: 159-170 [Abstract] [Full Text]
Pryzwansky, K. B., Merricks, E. P. (1998). Chemotactic Peptide-induced Changes of Intermediate Filament Organization in Neutrophils during Granule Secretion: Role of Cyclic Guanosine Monophosphate. Mol. Biol. Cell 9: 2933-2947 [Abstract] [Full Text]
Elliott, G., O'Hare, P. (1998). Herpes Simplex Virus Type 1�Tegument Protein VP22 Induces the Stabilization and Hyperacetylation of Microtubules. J. Virol. 72: 6448-6455 [Abstract] [Full Text]
Liao, G., Gundersen, G. G. (1998). Kinesin Is a Candidate for Cross-bridging Microtubules and Intermediate Filaments. SELECTIVE BINDING OF KINESIN TO DETYROSINATED TUBULIN AND VIMENTIN. J. Biol. Chem. 273: 9797-9803 [Abstract] [Full Text]
Rezniczek, G. A., de Pereda, J. M., Reipert, S., Wiche, G. (1998). Linking Integrin {alpha}6{beta}4-based Cell Adhesion to the Intermediate Filament Cytoskeleton: Direct Interaction between the {beta}4 Subunit and Plectin at Multiple Molecular Sites. JCB 141: 209-225 [Abstract] [Full Text]
Kong, J., Tung, V. W.-Y., Aghajanian, J., Xu, Z. (1998). Antagonistic Roles of Neurofilament Subunits NF-H and NF-M Against NF-L in Shaping Dendritic Arborization in Spinal Motor Neurons. JCB 140: 1167-1176 [Abstract] [Full Text]
Fuchs, E., Cleveland, D. W. (1998). A Structural Scaffolding of Intermediate Filaments in Health and Disease. Science 279: 514-519 [Abstract] [Full Text]
Wiche, G (1998). Role of plectin in cytoskeleton organization and dynamics. J. Cell Sci. 111: 2477-2486 [Abstract]
Ho, C., Martys, J., Mikhailov, A, Gundersen, G., Liem, R. (1998). Novel features of intermediate filament dynamics revealed by green fluorescent protein chimeras. J. Cell Sci. 111: 1767-1778 [Abstract]
Vilalta, P., Zhang, L, Hamm-Alvarez, S. (1998). A novel taxol-induced vimentin phosphorylation and stabilization revealed by studies on stable microtubules and vimentin intermediate filaments. J. Cell Sci. 111: 1841-1852 [Abstract]
Eckes, B, Dogic, D, Colucci-Guyon, E, Wang, N, Maniotis, A, Ingber, D, Merckling, A, Langa, F, Aumailley, M, Delouvee, A, Koteliansky, V, Babinet, C, Krieg, T (1998). Impaired mechanical stability, migration and contractile capacity in vimentin-deficient fibroblasts. J. Cell Sci. 111: 1897-1907 [Abstract]
Ruhrberg, C., Hajibagheri, M.A. N., Parry, D. A.D., Watt, F. M. (1997). Periplakin, a Novel Component of Cornified Envelopes and Desmosomes That Belongs to the Plakin Family and Forms Complexes with Envoplakin. JCB 139: 1835-1849 [Abstract] [Full Text]
Andra, K., Lassmann, H., Bittner, R., Shorny, S., Fassler, R., Propst, F., Wiche, G. (1997). Targeted inactivation of plectin reveals essential function in maintaining the integrity of skin, muscle, and heart�cytoarchitecture. Genes Dev. 11: 3143-3156 [Abstract] [Full Text]
Svitkina, T. M., Verkhovsky, A. B., McQuade, K. M., Borisy, G. G. (1997). Analysis of the Actin-Myosin II System in Fish Epidermal Keratocytes: Mechanism of Cell Body Translocation. JCB 139: 397-415 [Abstract] [Full Text]
Holwell, T., Schweitzer, S., Evans, R. (1997). Tetracycline regulated expression of vimentin in fibroblasts derived from vimentin null mice. J. Cell Sci. 110: 1947-1956 [Abstract]
Eger, A, Stockinger, A, Wiche, G, Foisner, R (1997). Polarisation-dependent association of plectin with desmoplakin and the lateral submembrane skeleton in MDCK cells. J. Cell Sci. 110: 1307-1316 [Abstract]
Maatta, A., Ruhrberg, C., Watt, F. M. (2000). Structure and Regulation of the Envoplakin Gene. J. Biol. Chem. 275: 19857-19865 [Abstract] [Full Text]
Russell, R. L., Cao, D., Zhang, D., Handschumacher, R. E., Pizzorno, G. (2001). Uridine Phosphorylase Association with Vimentin. INTRACELLULAR DISTRIBUTION AND LOCALIZATION. J. Biol. Chem. 276: 13302-13307 [Abstract] [Full Text]
Bellin, R. M., Huiatt, T. W., Critchley, D. R., Robson, R. M. (2001). Synemin May Function to Directly Link Muscle Cell Intermediate Filaments to Both Myofibrillar Z-lines and Costameres. J. Biol. Chem. 276: 32330-32337 [Abstract] [Full Text]
Stamenovic, D., Mijailovich, S. M., Tolic-Norrelykke, I. M., Chen, J., Wang, N. (2002). Cell prestress. II. Contribution of microtubules. Am. J. Physiol. Cell Physiol. 282: C617-C624 [Abstract] [Full Text]